AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Stress and Brain Article
PDF (2.5 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Exposure to single prolonged stress fails to induce anxiety-like behavior in mice

Wen-Jie You1,§, Ye He2,§, Wei-Zhu Liu1, Yu-Ge Zhu3, Ping Hu3, Bing-Xing Pan1, Wen-Hua Zhang1( )
Laboratory of Fear and Anxiety Disorders, Institute of Life Science, Nanchang University, Nanchang 330031, China
Center for Basic Medical Experiment, Nanchang University, Nanchang 330031, China
Institute of Translational Medicine, Nanchang University, Nanchang 330031, China

§ Wen-Jie You and Ye He contributed equally to this work.

Show Author Information

Graphical Abstract

Abstract

Single prolonged stress (SPS) is a well-established and most frequently used rat model to induce post-traumatic stress disorder (PTSD)-like symptoms, which helps to understand the neurobiological mechanisms as well as developing novel therapeutic strategies for PTSD. However, whether such stress model works efficiently in mice remains unknown. In the present study, we established a mouse SPS (mSPS) model by exposing C57BL/6J mice to a series of multimodal stressors on a single day, then the anxiety-like behavior was measured by open-field test, elevated plus maze test, dark-light box, and novelty-suppressed feeding test. Our results showed that mSPS had no significant effect on the anxiety-like behavior in mice after different days of recovery. The expression of the glucocorticoid receptor and brain-derived neurotrophic factor (BDNF), two proteins that highly associated with stress-related behaviors, also remained unaltered in both the amygdala and hippocampus. By contrast, the protein levels of NR2A and NR2B, two main subunits of the N-methyl-D-aspartate receptor (NMDAR), was reduced in the hippocampus, but not amygdala. In conclusion, our results indicate that mSPS may not be an efficient mouse model to explore the pathophysiology of PTSD-related anxiety-like behavior.

Keywords

post-traumatic stress disorder (PTSD)anxiety-like behaviorsingle prolonged stressmouseglucocorticoid receptorbrain-derived neurotrophic factor (BDNF)

References

[1]
Koenen, K. C., Ratanatharathorn, A., Ng, L., McLaughlin, K. A., Bromet, E. J., Stein, D. J., Karam, E. G., Meron Ruscio, A., Benjet, C., Scott, K. et al. Posttraumatic stress disorder in the world mental health surveys. Psychological Medicine, 2017, 47(13): 2260-2274.
Crossref Google Scholar
[2]
Abdallah, C. G., Southwick, S. M., Krystal, J. H. Neurobiology of posttraumatic stress disorder (PTSD): A path from novel pathophysiology to innovative therapeutics. Neuroscience Letters, 2017, 649: 130-132.
Crossref Google Scholar
[3]
Deslauriers, J., Toth, M., Der-Avakian, A., Risbrough, V. B. Current status of animal models of posttraumatic stress disorder: Behavioral and biological phenotypes, and future challenges in improving translation. Biological Psychiatry, 2018, 83(10): 895-907.
Crossref Google Scholar
[4]
Takei, S., Morinobu, S., Yamamoto, S., Fuchikami, M., Matsumoto, T., Yamawaki, S. Enhanced hippocampal BDNF/TrkB signaling in response to fear conditioning in an animal model of posttraumatic stress disorder. Journal of Psychiatric Research, 2011, 45(4): 460-468.
Crossref Google Scholar
[5]
Yamamoto, S., Morinobu, S., Takei, S., Fuchikami, M., Matsuki, A., Yamawaki, S., Liberzon, I. Single prolonged stress: Toward an animal model of posttraumatic stress disorder. Depression and Anxiety, 2009, 26(12): 1110-1117.
Crossref Google Scholar
[6]
Liberzon, I., Young, E. A. Effects of stress and glucocorticoids on CNS oxytocin receptor binding. Psychoneuroendocrinology, 1997, 22(6): 411-422.
Crossref Google Scholar
[7]
Han, F., Ding, J. L., Shi, Y. X. Expression of amygdala mineralocorticoid receptor and glucocorticoid receptor in the single-prolonged stress rats. BMC Neuroscience, 2014, 15(1): 77.
Crossref Google Scholar
[8]
Imanaka, A., Morinobu, S., Toki, S., Yamawaki, S. Importance of early environment in the development of post-traumatic stress disorder-like behaviors. Behavioural Brain Research, 2006, 173(1): 129-137.
Crossref Google Scholar
[9]
Bachmann, A. W., Sedgley, T. L., Jackson, R. V., Gibson, J. N., Young, R. M., Torpy, D. J. Glucocorticoid receptor polymorphisms and post-traumatic stress disorder. Psychoneuroendocrinology, 2005, 30(3): 297-306.
Crossref Google Scholar
[10]
Souza, R. R., Noble, L. J., McIntyre, C. K. Using the single prolonged stress model to examine the pathophysiology of PTSD. Frontiers in Pharmacology, 2017, .
Crossref Google Scholar
[11]
Martinowich, K., Manji, H., Lu, B. New insights into BDNF function in depression and anxiety. Nature Neuroscience, 2007, 10(9): 1089-1093.
Crossref Google Scholar
[12]
Paoletti, P., Bellone, C., Zhou, Q. NMDA receptor subunit diversity: Impact on receptor properties, synaptic plasticity and disease. Nature Reviews Neuroscience, 2013, 14(6): 383-400.
Crossref Google Scholar
[13]
Aikins, D. E., Strader, J. A., Kohler, R. J., Bihani, N., Perrine, S. A. Differences in hippocampal serotonergic activity in a mouse single prolonged stress paradigm impact discriminant fear acquisition and retention. Neuroscience Letters, 2017, 639: 162-166.
Crossref Google Scholar
[14]
Perrine, S. A., Eagle, A. L., George, S. A., Mulo, K., Kohler, R. J., Gerard, J., Harutyunyan, A., Hool, S. M., Susick, L. L., Schneider, B. L. et al. Severe, multimodal stress exposure induces PTSD-like characteristics in a mouse model of single prolonged stress. Behavioural Brain Research, 2016, 303: 228-237.
Crossref Google Scholar
[15]
Wang, H. F., Zuo, D. Y., He, B., Qiao, F. X., Zhao, M. Q., Wu, Y. L. Conditioned fear stress combined with single-prolonged stress: A new PTSD mouse model. Neuroscience Research, 2012, 73(2): 142-152.
Crossref Google Scholar
[16]
Zhang, W. H., Liu, W. Z., He, Y., You, W. J., Zhang, J. Y., Xu, H., Tian, X. L., Li, B. M., Mei, L., Holmes, A. et al. Chronic stress causes projection-specific adaptation of amygdala neurons via small-conductance calcium-activated potassium channel downregulation. Biological Psychiatry, 2019, 85(10): 812-828.
Crossref Google Scholar
[17]
Zhang, W. H., Zhou, J., Pan, H. Q., Wang, X. Y., Liu, W. Z., Zhang, J. Y., Yin, X. P., Pan, B. X. δ Subunit-containing GABAA receptor prevents overgeneralization of fear in adult mice. Learning & Memory (Cold Spring Harbor, N.Y.), 2017, 24(8): 381-384.
Crossref Google Scholar
[18]
Zhang, J. Y., Liu, T. H., He, Y., Pan, H. Q., Zhang, W. H., Yin, X. P., Tian, X. L., Li, B. M., Wang, X. D., Holmes, A. et al. Chronic stress remodels synapses in an amygdala circuit-specific manner. Biological Psychiatry, 2019, 85(3): 189-201.
Crossref Google Scholar
[19]
Eagle, A. L., Knox, D., Roberts, M. M., Mulo, K., Liberzon, I., Galloway, M. P., Perrine, S. A. Single prolonged stress enhances hippocampal glucocorticoid receptor and phosphorylated protein kinase B levels. Neuroscience Research, 2013, 75(2): 130-137.
Crossref Google Scholar
[20]
Knox, D., Nault, T., Henderson, C., Liberzon, I. Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model. Neuroscience, 2012, 223: 163-173.
Crossref Google Scholar
[21]
Cao, B., Ni, H. Y., Li, J., Zhou, Y., Bian, X. L., Tao, Y., Cai, C. Y., Qin, C., Wu, H. Y., Chang, L. et al. (+)-Borneol suppresses conditioned fear recall and anxiety-like behaviors in mice. Biochemical and Biophysical Research Communications, 2018, 495(2): 1588-1593.
Crossref Google Scholar
[22]
Barbazanges, A., Piazza, P. V., Le Moal, M., Maccari, S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. The Journal of Neuroscience, 1996, 16(12): 3943-3949.
Crossref Google Scholar
[23]
Bentefour, Y., Bennis, M., Garcia, R., M’hamed, S. B. Effects of paroxetine on PTSD-like symptoms in mice. Psychopharmacology, 2015, 232(13): 2303-2312.
Crossref Google Scholar
[24]
Schöner, J., Heinz, A., Endres, M., Gertz, K., Kronenberg, G. Post-traumatic stress disorder and beyond: An overview of rodent stress models. Journal of Cellular and Molecular Medicine, 2017, 21(10): 2248-2256.
Crossref Google Scholar
[25]
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., Chattarji, S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. PNAS, 2005, 102(26): 9371-9376.
Crossref Google Scholar
[26]
Golden, S. A., Covington, H. E. III, Berton, O., Russo, S. J. A standardized protocol for repeated social defeat stress in mice. Nature Protocols, 2011, 6(8): 1183-1191.
Crossref Google Scholar
[27]
Lisieski, M. J., Eagle, A. L., Conti, A. C., Liberzon, I., Perrine, S. A. Single-prolonged stress: A review of two decades of progress in a rodent model of post-traumatic stress disorder. Frontiers in Psychiatry, 2018, 9: 196.
Crossref Google Scholar
[28]
Barkus, C., McHugh, S. B., Sprengel, R., Seeburg, P. H., Rawlins, J. N. P., Bannerman, D. M. Hippocampal NMDA receptors and anxiety: At the interface between cognition and emotion. European Journal of Pharmacology, 2010, 626(1): 49-56.
Crossref Google Scholar
[29]
Harvey, B. H., Stein, D. J., Oosthuizen, F., Brand, L., Wegener, G. Stress-restress evokes sustained iNOS activity and altered GABA levels and NMDA receptors in rat hippocampus. Psychopharmacology, 2004, 175: 494-502.
Google Scholar
[30]
Harvey, B. H., Naciti, C., Brand, L., Stein, D. J. Endocrine, cognitive and hippocampal/cortical 5HT1A/ 2A receptor changes evoked by a time-dependent sensitisation (TDS) stress model in rats. Brain Research, 2003, 983(1-2): 97-107.
Crossref Google Scholar
[31]
Keller-Wood, M. Hypothalamic-pituitary-adrenal axis—feedback control. Comprehensive Physiology, 2015 5(3): 1161-1182.
Crossref Google Scholar
[32]
Tasker, J. G., Herman, J. P. Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic-pituitary-adrenal axis. Stress, 2011, 14(4): 398-406.
Crossref Google Scholar
[33]
Ott, T., Nieder, A. Dopamine and cognitive control in prefrontal cortex. Trends in Cognitive Sciences, 2019, 23(3): 213-234.
Crossref Google Scholar
[34]
Kinlein, S. A., Phillips, D. J., Keller, C. R., Karatsoreos, I. N. Role of corticosterone in altered neurobehavioral responses to acute stress in a model of compromised hypothalamic-pituitary-adrenal axis function. Psychoneuroendocrinology, 2019, 102: 248-255.
Crossref Google Scholar
[35]
Myers, B., McKlveen, J. M., Herman, J. P. Glucocorticoid actions on synapses, circuits, and behavior: Implications for the energetics of stress. Frontiers in Neuroendocrinology, 2014, 35(2): 180-196.
Crossref Google Scholar
[36]
Ganon-Elazar, E., Akirav, I. Cannabinoids and traumatic stress modulation of contextual fear extinction and GR expression in the amygdala-hippocampal-prefrontal circuit. Psychoneuroendocrinology, 2013, 38(9): 1675-1687.
Crossref Google Scholar
[37]
Du, Z., Han, F., Shi, Y. X. Expressions of hippocampal mineralocorticoid receptor (MR) and glucocorticoid receptor (GR) in the single-prolonged stress-rats. Acta Histochemica et Cytochemica, 2008, 41(4): 89-95.
Crossref Google Scholar
[38]
Liberzon, López, Flagel, Vázquez, Young. Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: Relevance to post-traumatic stress disorder. Journal of Neuroendocrinology, 1999, 11(1): 11-17.
Crossref Google Scholar
[39]
Lakshminarasimhan, H., Chattarji, S. Stress leads to contrasting effects on the levels of brain derived neurotrophic factor in the hippocampus and amygdala. PLoS One, 2012, 7(1): e30481.
Crossref Google Scholar
[40]
Chen, B., Dowlatshahi, D., MacQueen, G. M., Wang, J. F., Young, L. T. Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biological Psychiatry, 2001, 50(4): 260-265.
Crossref Google Scholar
Stress and Brain
Volume 1 Issue 2,
December 2021
Pages 145-159
DOI: 10.26599/SAB.2020.9060001
Cite this article:
You W-J, He Y, Liu W-Z, et al. Exposure to single prolonged stress fails to induce anxiety-like behavior in mice. Stress and Brain, 2021, 1(2): 145-159. https://doi.org/10.26599/SAB.2020.9060001

3954

Views

491

Downloads

3

Crossref

Altmetrics
Received: 11 January 2020
Revised: 28 July 2020
Accepted: 27 October 2020
Published: 01 February 2021
© The Author(s) 2020

Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission.
Return